Merendino, L. | bioRxiv Science

bioRxiv2024

Early seedling development in dark conditions is directly controlled by plastids through the GUN1-dependent plastid retrograde pathway

In dark growth conditions, seedlings develop specific features such as an elongated hypocotyl, a tightly folded apical hook, and non-green cotyledons. This dark-specific process, known as skotomorphogenesis, relies primarily on mitochondria and eventually etioplasts for energy. Our previous research shows that skotomorphogenesis is reprogrammed in response to mitochondrial and plastidial dysfunction. Even though the direct link between mitochondria and skotomorphogenesis was described, the impact of plastid dysfunction on early development could not be separated from mitochondrial stress. In this study, we aim to determine the direct connection between plastid functionality and skotomorphogenic response. In this situation, we analyze the phenotypic, molecular, and metabolic effects of treating etiolated seedlings using lincomycin and spectinomycin, which target plastid translation. Our results with the lincomycin treatment highlight the direct role of plastids in the control of early development, even in dark growth conditions, in the absence of any photosynthetic activity, and without the involvement of mitochondrial intermediates. Additionally, our findings suggest that GUN1 plays a regulatory role in regulating nuclear gene expression in response to plastid translation inhibition. Thanks to our study, we can now build a more precise model proposing a straight link between the reprogramming of early development and the dysfunction of plastids in dark-growth conditions. Significance statementIn underground germination conditions, seedlings follow a dark-specific development program, called skotomorphogenesis, that is required for their efficient emergence from the soil. Our study demonstrates that plastids play a crucial role in controlling skotomorphogenesis, even in the absence of photosynthetic activity and without affecting mitochondrial function, and therefore we propose that regulation of etioplast functions might contribute to the adaptation of seedling development to constraining environmental conditions.

plant biology↗

bioRxiv2022

Limiting etioplast gene-expression induces apical hook twisting during skoto-morphogenesis of Arabidopsis seedlings

When covered by a layer of soil, seedling development follows a dark-specific program (skoto-morphogenesis) consisting of small, non-green cotyledons, a long hypocotyl and an apical hook to protect meristematic cells. We recently highlighted the role played by mitochondria in the high energy-consuming reprogramming of Arabidopsis skoto-morphogenesis. Here, the role played by plastids, another energy supplying organelle, in skoto-morphogenesis is investigated. This study was conducted in dark conditions to exclude light signals so as to better focus on those produced by plastids. It was found that limitation of plastid gene-expression (PGE) induced an exaggerated apical hook bending. Inhibition of PGE was obtained at the level of transcription and translation using the antibiotics rifampicin and spectinomycin, respectively, as well as plastid RPOTP RNA polymerase mutants. Rifampicin-treated seedlings also showed expression induction of marker nuclear genes for mitochondrial stress, perturbation of the mitochondrial metabolism, increase of ROS levels and an augmented capacity of oxygen consumption by mitochondrial alternative oxidases (AOX). AOX enzymes act to prevent over-reduction of the mitochondrial electron transport chain. Previously, we reported that AOX1A, the main AOX isoform, was a key component in the developmental response to mitochondrial respiration deficiency. In this work, we suggest the involvement of AOX1A in the response to PGE dysfunction and propose the importance of signalling between plastids and mitochondria. Finally, it was found that seedling architecture reprogramming in response to rifampicin was independent of canonical organelle retrograde pathways and the ethylene signaling pathway. Significance statementIn underground germination conditions, seedling development follows a dark-specific program (skoto-morphogenesis) consisting of small and non-green cotyledons, a long hypocotyl and an apical hook to protect meristematic cells. We show that skoto-morphogenesis is reprogrammed when plastid gene expression is perturbed leading to an exaggeration of apical hook bending. We propose the involvement of the cooperation between plastids and mitochondria, the energy-supplying organelles of the cell.

plant biology↗